Bdellovibrio bacteriovorus uses chimeric fibre proteins to recognize and invade a broad range of bacterial hosts

Simon G Caulton; Carey Lambert; Jess Tyson; Paul Radford; Asmaa Al-Bayati; Samuel Greenwood; Emma J Banks; Callum Clark; Rob Till; Elisabete Pires; R. Elizabeth Sockett; Andrew Lovering

doi:10.1038/s41564-023-01552-2

Bdellovibrio bacteriovorus uses chimeric fibre proteins to recognize and invade a broad range of bacterial hosts

Simon G Caulton, Carey Lambert, Jess Tyson, Paul Radford, Asmaa Al-Bayati, Samuel Greenwood, Emma J Banks, Callum Clark, Rob Till, Elisabete Pires, R. Elizabeth Sockett^*, Andrew Lovering^*

^*Corresponding author for this work

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Abstract

Predatory bacteria, like the model endoperiplasmic bacterium Bdellovibrio bacteriovorus, show several adaptations relevant to their requirements for locating, entering and killing other bacteria. The mechanisms underlying prey recognition and handling remain obscure. Here we use complementary genetic, microscopic and structural methods to address this deficit. During invasion, the B. bacteriovorus protein CpoB concentrates into a vesicular compartment that is deposited into the prey periplasm. Proteomic and structural analyses of vesicle contents reveal several fibre-like proteins, which we name the mosaic adhesive trimer (MAT) superfamily, and show localization on the predator surface before prey encounter. These dynamic proteins indicate a variety of binding capabilities, and we confirm that one MAT member shows specificity for surface glycans from a particular prey. Our study shows that the B. bacteriovorus MAT protein repertoire enables a broad means for the recognition and handling of diverse prey epitopes encountered during bacterial predation and invasion.

Original language	English
Pages (from-to)	214-227
Number of pages	14
Journal	Nature Microbiology
Volume	9
Issue number	1
DOIs	https://doi.org/10.1038/s41564-023-01552-2
Publication status	Published - 4 Jan 2024

Bibliographical note

Acknowledgements:
S.G.C., C.L., A.L.L., R.E.S., P.R. and J.T. were funded by the Wellcome Trust Investigator Award in Science (209437/Z/17/Z). For the purposes of open access, R.E.S. and A.L.L. have applied a CC BY public copyright licence for the author-accepted manuscript version arising from this submission. R.T. was partially funded by the same award and partly by the University of Nottingham. A.A.-B. was funded by PhD studentship from the Government of Iraq. S.G. was a self-funded University of Nottingham undergraduate student. E.J.B. and C.C. were funded by Wellcome Trust PhD studentships (215025/Z/18/Z and 220105/Z/20/Z, respectively) and University of Nottingham and Birmingham AAMR DTP Scheme 108876/Z/15/Z. E.P. was funded for this proteomic analysis by a subcontract from the Oxford Advanced Proteomics Unit, University of Oxford, UK.

Copyright:
© 2024. The Author(s).

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10.1038/s41564-023-01552-2Licence: Creative Commons: Attribution (CC BY)

CaultonS2024BdellovibrioFinal published version, 5.04 MBLicence: Creative Commons: Attribution (CC BY)

Combating Gram Negative AMR Pathogens by Understanding the Envelope-Breaching Mechanisms of Predatory Bacteria
Lovering, A.
THE WELLCOME TRUST
1/03/18 → 30/04/24
Project: Research

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title = "Bdellovibrio bacteriovorus uses chimeric fibre proteins to recognize and invade a broad range of bacterial hosts",

abstract = "Predatory bacteria, like the model endoperiplasmic bacterium Bdellovibrio bacteriovorus, show several adaptations relevant to their requirements for locating, entering and killing other bacteria. The mechanisms underlying prey recognition and handling remain obscure. Here we use complementary genetic, microscopic and structural methods to address this deficit. During invasion, the B. bacteriovorus protein CpoB concentrates into a vesicular compartment that is deposited into the prey periplasm. Proteomic and structural analyses of vesicle contents reveal several fibre-like proteins, which we name the mosaic adhesive trimer (MAT) superfamily, and show localization on the predator surface before prey encounter. These dynamic proteins indicate a variety of binding capabilities, and we confirm that one MAT member shows specificity for surface glycans from a particular prey. Our study shows that the B. bacteriovorus MAT protein repertoire enables a broad means for the recognition and handling of diverse prey epitopes encountered during bacterial predation and invasion.",

author = "Caulton, {Simon G} and Carey Lambert and Jess Tyson and Paul Radford and Asmaa Al-Bayati and Samuel Greenwood and Banks, {Emma J} and Callum Clark and Rob Till and Elisabete Pires and Sockett, {R. Elizabeth} and Andrew Lovering",

note = "Acknowledgements: S.G.C., C.L., A.L.L., R.E.S., P.R. and J.T. were funded by the Wellcome Trust Investigator Award in Science (209437/Z/17/Z). For the purposes of open access, R.E.S. and A.L.L. have applied a CC BY public copyright licence for the author-accepted manuscript version arising from this submission. R.T. was partially funded by the same award and partly by the University of Nottingham. A.A.-B. was funded by PhD studentship from the Government of Iraq. S.G. was a self-funded University of Nottingham undergraduate student. E.J.B. and C.C. were funded by Wellcome Trust PhD studentships (215025/Z/18/Z and 220105/Z/20/Z, respectively) and University of Nottingham and Birmingham AAMR DTP Scheme 108876/Z/15/Z. E.P. was funded for this proteomic analysis by a subcontract from the Oxford Advanced Proteomics Unit, University of Oxford, UK. Copyright: {\textcopyright} 2024. The Author(s).",

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doi = "10.1038/s41564-023-01552-2",

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AU - Al-Bayati, Asmaa

AU - Greenwood, Samuel

AU - Banks, Emma J

AU - Clark, Callum

AU - Till, Rob

AU - Pires, Elisabete

AU - Sockett, R. Elizabeth

AU - Lovering, Andrew

N1 - Acknowledgements: S.G.C., C.L., A.L.L., R.E.S., P.R. and J.T. were funded by the Wellcome Trust Investigator Award in Science (209437/Z/17/Z). For the purposes of open access, R.E.S. and A.L.L. have applied a CC BY public copyright licence for the author-accepted manuscript version arising from this submission. R.T. was partially funded by the same award and partly by the University of Nottingham. A.A.-B. was funded by PhD studentship from the Government of Iraq. S.G. was a self-funded University of Nottingham undergraduate student. E.J.B. and C.C. were funded by Wellcome Trust PhD studentships (215025/Z/18/Z and 220105/Z/20/Z, respectively) and University of Nottingham and Birmingham AAMR DTP Scheme 108876/Z/15/Z. E.P. was funded for this proteomic analysis by a subcontract from the Oxford Advanced Proteomics Unit, University of Oxford, UK. Copyright: © 2024. The Author(s).

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N2 - Predatory bacteria, like the model endoperiplasmic bacterium Bdellovibrio bacteriovorus, show several adaptations relevant to their requirements for locating, entering and killing other bacteria. The mechanisms underlying prey recognition and handling remain obscure. Here we use complementary genetic, microscopic and structural methods to address this deficit. During invasion, the B. bacteriovorus protein CpoB concentrates into a vesicular compartment that is deposited into the prey periplasm. Proteomic and structural analyses of vesicle contents reveal several fibre-like proteins, which we name the mosaic adhesive trimer (MAT) superfamily, and show localization on the predator surface before prey encounter. These dynamic proteins indicate a variety of binding capabilities, and we confirm that one MAT member shows specificity for surface glycans from a particular prey. Our study shows that the B. bacteriovorus MAT protein repertoire enables a broad means for the recognition and handling of diverse prey epitopes encountered during bacterial predation and invasion.

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JO - Nature Microbiology

JF - Nature Microbiology

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Bdellovibrio bacteriovorus uses chimeric fibre proteins to recognize and invade a broad range of bacterial hosts

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Combating Gram Negative AMR Pathogens by Understanding the Envelope-Breaching Mechanisms of Predatory Bacteria

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